Diet of the Assamese Macaque Macaca Assamensis in Lime- Stone Habitats of Nonggang, China

Current Zoology 57 (1): 18−25, 2011

Diet of the Assamese macaque Macaca assamensis in limestone habitats of Nonggang, China

Qihai ZHOU1, Hua WEI1, 2, Zhonghao HUANG1, Chengming HUANG1, 3*

1 Key Laboratory of Ecology of Rare and Endangered Species and Environment Protection (Gangxi Normal University), Ministry of Education, Guilin 541004, China. 2 The Zoo of Seven Star Park, Guilin 541004, China 3 Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

Abstract To enhance our understanding of dietary adaptations in macaques we studied the diet of the Assamese macaque Macaca assamensis in limestone seasonal rain forests at Nonggang Nature Reserve, China from September 2005 to August 2006. Our results show that although macaques fed on many plant species, 85.2% of the diet came from only 12 species, of which a bamboo species, Indocalamus calcicolus contributed to 62% of the diet. Young leaves were staple food items (74.1% of the diet) for Assamese macaques at Nonggang, and constituted the bulk of monthly diets almost year-round, ranging from 44.9% (July) to 92.9% (May). Young parts of Indocalamus calcicolus unexpanded leaves contributed to a large proportion of the young leaf diet in most months. Fruit accounted for only 17.4% of the diet, with a peak of consumption in July. We suggest that this highly folivorous diet may be related to the long lean season of fruit availability in limestone habitats as well as the utilization of cliffs of low fruit availability [Current Zoology 57 (1): 18–25, 2011]. Key words Assamese macaque, Macaca assamensis, Diet, Limestone habitat

Many studies have revealed dietary variation among sified as Near Threatened by the 2008 IUCN Red List primates (Campbell et al., 2007; Yeager and Koll, 2000). (Boonratana et al., 2008). They are distributed in Nepal, Macaque species have been described as primarily Sikkim, Bhutan, India, northern Thailand, and south- frugivorous (Caldecott, 1986; Yeager, 1996; O’Brien ernmost China (to the upper Mekong in Tibet, and in the and Kinnaird, 1997; Andrews, 2003; Riley, 2007). For east into southern Guizhou). They live in many different example, O’Brien and Kinnaird (1997) reported that habitats including monsoon evergreen broadleaf forest, crested black macaques Macaca nigra spent 66% of deciduous broadleaf forest, mixed broadleaf and conifer feeding time on fruits. A study of tonkean macaques M. forest, and conifer forest (Zhang et al., 1997). Some tonkeana in Sulawesi, Indonesia, showed that fruits ac- studies have been undertaken on the diet of Assamese counted for 76.7%-84.4% of their diets (Riley, 2007). macaques in the highlands of Nepal, Bhutan and India, However, evidence is steadily accumulating that leaves and have concluded that they are primarily folivorous contribute a large proportion of diet in some species (Ahsan, 1994; Chalise et al., 2003). However, system- (Zhao, 1996; Hanya, 2004). For example, Japanese ma- atic study on the behavior and ecology of this species in caques M. fuscata in the coniferous forest of Yakushima China is rare, which is important for supplementing the spent 45% of feeding time on leaves, and feeding time on biology of the species, and also provide comparative fruits was only 13% (Hanya, 2004). Even within a spe- information for the general study of behavioral adapta- cies and population, considerable dietary variation in tion in macaques. Here, we present data on the diet of terms of plant species and parts eaten may occur (Hanya Assamese macaques at Nonggang Nature Reserve, et al., 2003; Harris and Chapman, 2007). For example, southern China. We first summarize data on dietary Hanya et al. (2003) found variation in diet amongst Japa- composition, and then describe seasonal changes in diet. nese macaques inhabiting different altitudinal zones. Much 1 Materials and Methods of these differences can largely be explained as differences in the temporal availability and spatial distribution of fruit 1.1 Study site and animal resources (Hanya et al., 2003; Hanya, 2004). Nonggang Nature Reserve is located in southwest The Assamese macaque Macaca assamensis is clas- Guangxi province, China (106°42′–107°4′E, 22°13′–

22°33′N), and comprises three areas, Nonggang (5426 ability. Most large fruiting trees are found in valley ba- ha), Longhu (1034 ha), and Longshan (3949 ha), sepa- sins and on hillsides rich in wet soil. The cliffs and hill- rated by farmlands and villages. The reserve consists of tops consist of bare rock, and are covered by small limestone hills with elevations 300-700 m above sea drought-enduring trees (Liang et al., 1988). Annual pre- level (Guangxi Forestry Department, 1993). Our re- cipitation during the study period (September search site lies in northwestern of Nonggang (Fig. 1). 2005–August 2006) was 1372 mm. The area encounters Vegetation is characterized as limestone seasonal rain two seasons, a rainy season from April and September forest (Shu et al., 1988). Vegetation differs across the with > 80 mm monthly rainfall and a dry season with < area due to differences in soil and surface water avail- 80 mm monthly rainfall (Fig. 2).

Fig. 1 Nonggang Nature Reserve showing the study site and surrounding area

Fig. 2 Monthly rainfall and abundance of young leaves, fruit and flowers at Nonggang Nature Reserve between September 2005 and August 2006 20 Current Zoology Vol. 57 No. 1

At least six social groups of Assamese macaques in- petiole, root and bark). If possible, specimens of plant habit the study area. In this study, most behavioral data species eaten were collected for later identification by were collected from Group 1 and Group 2 who ranged the Institute of Botany, Chinese Academy of Sciences nearest to our temporary camp. Group 1 consisted of 15 (Guilin, Guangxi). individuals (two adult males, four adult females, four 1.4 Data analysis adult individuals of unidentified sex, and five juveniles) We expressed the relative availability of different at the start of this study, and increased to 17 individuals plant parts as the percentage of trees bearing the plant due to the birth of two infants in June 2006. Group 2 parts of interest each month, regardless of the size of the had 12 individuals (two adult males, four adult females, canopy. The percentage of time spent consuming each two adult individuals of unidentified sex, and four juve- plant species was calculated from the number of feeding niles) at the start of this study and two infants were born records for plant species divided by the total number of in June and July 2006. feeding records. Monthly diet composition was ex- 1.2 Ecological sampling pressed as the percentage of feeding records devoted to We conducted vegetation surveys at the onset of be- different food items among monthly total feeding re- havioral data collection. We used a stratified random cords. Annual diet composition was obtained by aver- sampling method for placement of vegetation plots. We aging monthly percentages. We excluded records for placed 13 plots (50 m×10 m) in the main study area, dependent infants and juveniles (n = 200) from analysis including four at valley basins and nine on hillsides. The because they were not foraging independently and in- plots covered most of the vegetation types described by fant and juvenile mouthing of prospective foods often Shu et al. (1988). Within plots we tagged all trees with a cannot be differentiated from actual feeding. diameter ≥ 5 cm at breast height (DBH), and meas- We used a Spearman rank correlation coefficient test ured DBH. Each month we visually inspected all tagged was used to examine correlations between the availabil- trees for the presence of young leaves, fruit, and flowers ity of plant parts of interest and rainfall. A Wilcoxon to evaluate seasonal changes in the availability of po- signed-rank test was used to examine inter-group varia- tential food resources. tion in the overall pattern of use of different plant parts. 1.3 Behavioral observation Because few records were collected in September and Field observations were done from September 2005 October 2005 we excluded data in these months for to August 2006. Because of difficult land physiognomy, comparisons of inter-group variations and later analysis. we were unable to conduct full-day consecutive behav- We used Mann-Whitney’s U test to examine seasonal ioral sampling for most days. Each sampling day, data variation in the availability of plant parts of interest and collection began when the monkeys were first encoun- the consumption of various items. All tests were two tered and ended when the monkeys disappeared or en- tailed, with significance levels of 0.05. tered sleeping sites. Instantaneous scan sampling was 2 Results used (Altmann, 1974). Scans lasted 5 min, followed by 10 min of inactivity until the next scan began. We re- 2.1 Phenology corded the activity of each individual seen during each A total of 312 trees of 56 species were monitored scan. We watched each individual for 5 s after detection within 13 vegetation plots. The availability of young and recorded its predominant behavior during that in- leaves and flowers reached their highest level in April terval. To avoid sampling bias toward certain individu- 2006. A peak of fruit availability was observed in June als of a particular age-sex class, we collected behavioral and July 2006 (Fig. 2). Compared to the dry season, the records on as many different individuals as possible availability of young leaves, fruits and flowers was during a scan so that all individuals in the focal group higher in the rainy season, but only the difference in the were included but we sampled no individual more than availability of fruit was statistically significant (young once. Because some individuals inevitably could not be leaf: Z = -1.604, n1 = 6, n2 = 6, P = 0.109; fruit: Z = found because of the dense vegetation, only a fraction of -2.330, P = 0.020; flower: Z = -0.855, P = 0.393). A the group could be sampled during most scans. significant and positive correlation was found between

We classified five general activities: resting, moving, monthly fruit availability and rainfall (rs = 0.719, n = 12, feeding, social grooming, and playing. When monkeys P = 0.008) were feeding we recorded the plant part eaten, including 2.2 Food plant species young leaf, mature leaf, fruit, flower, and others (e.g. During the study period a total of 6525 behavior re- ZHOU QH et al.: Diet of the Assamese macaque 21 cords were obtained from 1666 scan samples, with an pionurus sylvestris, and Sapium rotundifolium ac- average of 3.9 individuals per scan. We made 1259 counted for >1% each of all feeding records, and con- feeding records (monthly mean = 122, SD = 95, range = tributed to 85.2% of the total diet (Table 1). Of these 12 65 to 324), of which there were 1094 records of identi- species, Indocalamus calcicolus accounted for 62.0% of fied food species, and 1198 for identified food items. the total diet. Thus, the macaques concentrated on a few Macaques were observed to forage on 69 plant species species, but opportunistically consumed a large number (Table 1). Not counting eight unidentified species, the of other plant species. range of food included 34 families, 59 species of tree, 2.3 Food items eight species of vine, and two species of herb. Tree spe- Because there was no significant difference in diet cies accounted for 93.2% of total feeding records, vines between the two main study groups (Z = -0.674, n = 5, P for 3.1%, and herbs for 3.7%. = 0.500) we pooled their dietary data for analysis. As- Though the macaques consumed a large number of samese macaques were highly folivorous, and young plant species, only 12 species such as Indocalamus cal- leaves accounted for 74.1% of the total diet, of which cicolus, Ficus nervosa, Guihaia argyrata, Sinosider- young parts of Indocalamus calcicolus unexpanded oxylon pedunculatum, Canthium dicoccum, Burretio- leaves contributed to 77.7% of feeding records for dendron hsienmu, Croton euryphyllus, Ficus micro- young leaves (Fig. 3). Fruit accounted for 17.4% of the carpa, Ventilago calyculata, Berchemia floribunda, Le- total diet, and the majority of fruit in the diet came from

Table 1 Plant species consumed by Assamese macaques at Nonggang Nature Reserve between September 2005 and August 2006

Family Species Life form Parts eatena Number of month used %(F)b Vitaceae Ampelopsis brevipedunculata Vine FR 1 0.09 Ampelopsis cantoniensis Vine FR 1 0.46 Tetrastigma planicaule Vine YL,ST 1 0.36 Verbenaceae Vitex kwangsiensis Tree FR 1 0.09 Ulmaceae Trema cannabina Tree YL 1 0.09 Tiliaceae Burretiodendron hsienmu Tree YL 5 1.55 Hainania trichosperma Tree YL 2 0.46 Symplocaceae Symplocos decora Tree YL 1 0.18 Sterculiaceae Sterculialanceolata Tree YL,P 2 0.36 Smilacaceae Smilax ferox Tree ML 1 0.09 Sapotaceae Lepionurus sylvestris Tree YL.ML 5 1.18 Mastichodendron wightianum Tree YL 1 0.27 Sinosideroxylon pedunculatum Tree YL,FR 9 3.55 Sapindaceae Boniodendron minus Tree YL 4 0.73 Delavaya toxocarpa Tree FR 1 0.27 Sabiaceae Sabia swinhoei Tree YL.ML 2 0.64 Rubiaceae Adina racemosa Tree YL,F,B 3 0.46 Canthium dicoccum Tree YL,ML,FR,F 8 2.28 Rhamnaceae Berchemia floribunda Tree YL,F,P 4 1.37 Sageretia theezans Tree YL 1 0.18 Species 1 Tree FR 1 0.09 Ventilago calyculata Vine YL 4 1.37 Pinaceae Keteleeria fortunei Tree FR 1 0.09 Palmae Caryota ochlandra Tree FR 1 0.18 Guihaia argyrata Herb F,P 8 3.64

Myrsinaceae Embelia scandens Vine YL 1 0.09 (to be continued on the next page) 22 Current Zoology Vol. 57 No. 1

Table 1 (Continued)

Family Species Life form Parts eatena Number of month used %(F)b Schefflera glomerulata Tree YL 1 0.09 Moraceae Ficus cyrtophylla Tree FR 2 0.46 Ficus gibbosa Tree FR 2 0.46 Ficus glaberrima Tree FR 1 0.09 Ficus microcarpa Tree YL,FR 7 1.46 Ficus nervosa Tree YL,ML,FR,F 11 4.01 Ficus sp. Tree FR 2 0.36 Ficus sp. Tree FR 1 0.09 Ficus virens Tree FR 2 0.27 Ficus wightiana Tree YL,FR,P 4 0.91 Pseudostreblus indica Tree FR 1 0.18 Species 2 Tree YL 1 0.18 Mimosaceae Acacia pennata Tree S 1 0.18 Menispermaceae Diploclisia glaucescens Vine YL 1 0.09 Meliacea Aphanamixis grandifolia Tree YL,FR 2 0.55 Species 3 Tree FR 1 0.27 Melastomataceae Memecylon scutellatum Tree FR 1 0.09 Linaceae Tirpitzia ovoidea Tree FR 1 0.18 Leguminosae Pithecellobium clypearia Tree YL 1 0.09 Lauraceae Cinnamomum saxatile Tree YL,P 3 0.55 Icacinaceae Apodytes dimidiata Tree YL,FR 2 0.18 Lodes ovalis Vine FR 3 0.55 Guttifceae Garcinia paucinervis Tree P 3 0.82 Gramineae Species 4 Herb S 1 0.09 Fagaceae Quercus glauca Tree FR 1 0.09 Euphorblaceae Alchornea trewioides Tree FR 1 0.09 Bischofia javanica Tree YL 1 0.09 Croton euryphyllus Tree YL 4 1.55 Sapium rotundifolium Tree FR 4 1.18 Species 5 Tree FR 1 0.09 Trigonostemon thyrsoideus Tree YL 1 0.09 Ebenaceae Diospyros siderophyllus Tree FR 4 0.46 Bambusoideae Dendrocalamus minor Tree YL 2 0.18 Indocalamus calcicolus Tree YL 12 62.02 Phyllostachys bambusoides Tree YL 1 0.09 Aristolochiaceae Aristolochia cinnabaria Vine R 1 0.09 Araliaceae Schefflera octophylla Tree YL 2 0.18 Apocynaceae Trachelospermum brevistylum Tree YL,FR 5 0.73 Anacardiaceae Pistacia weinmannifolia Tree YL 1 0.09 Species 6 Tree YL 1 0.18 Alangiaceae Alangium chinense Tree YL 1 0.18 Species 7 Herb F 2 0.18 Species 8 Tree YL 1 0.09 a Parts eaten: YL, young leaf; ML, mature leaf; FR, fruit; S, seed; F, flower; P, petiole; ST, stem. b %(F): percentage of total feeding records ZHOU QH et al.: Diet of the Assamese macaque 23

calamus calcicolus unexpanded leaves contributed a large proportion of the young leaf diet in most months except for February, April and May (Fig. 4). Macaques ate more fruit when it was abundant in the rainy season, with peak consumption in July, but no significant seasonal variation was found in fruit consumption (Z = -0.838, P = 0.421). The consumption of flowers also showed no significant seasonal variation (Z = -0.105, P = 0.917), and was even across months, except for July and August, in which there was no feeding record for flowers. Although there was no significant seasonal variation in the consumption of mature leaves (Z = -1.509, P = 0.131), mature leaf consumption concen-

trated in the dry season months, with a peak in February. Macaques significantly increased the consumption of Fig. 3 Annual diet composition for Assamese macaques at Nonggang Nature Reserve other items (e.g. petiole, root and bark) in the dry season than in the rainy season (Z = -2.117, P = 0.034) (Fig. 4). four plant species: Ficus nervosa, Ficus microcarpa, 3 Discussion Sinosideroxylon pedunculatum, and Canthium dicoccum, which accounted for 55.7% of fruit feeding records. The The diet of Assamese macaques at Nonggang Nature consumption of mature leaves, flowers and other items Reserve was highly folivorous. Leaves accounted for (petioles, barks and roots) was low and accounted for 77.4% of total feeding records, whereas fruit only con- 3.3%, 2.7% and 2.5%, respectively. stituted 17.4% of total feeding records. This pattern is in 2.4 Seasonal Changes in Food Items accordance with reports from other study sites (Ahsan, Young leaves constituted the bulk of Assamese ma- 1994; Chalise et al., 2003). For example, the diet of As- caque monthly diet almost year-round, ranging from samese macaques in Bangladesh comprised more leaves 44.9% in July to 92.9% in May (Fig. 4), and their con- (46%) than fruit (23%) (Ahsan, 1994). Chalise et al. sumption showed no significant seasonal variation (Z = (2003) also reported that Assamese macaques in Nepal

-0.313, n1 = 5, n2 = 5, P = 0.754). Young parts of Indo- were predominately leaf eaters.

Fig. 4 Monthly percentage of feeding records devoted to different food items for Assamese macaques between November 2005 and August 2006 24 Current Zoology Vol. 57 No. 1

Although our study site is located in a sub-tropical nutritional quality such as for protein and are lower in area (Guangxi Forestry Department, 1993), fruit con- fiber and secondary compounds (Richard, 1985). sumption of Assamese macaques at Nonggang is much Although the availability of young leaves decreased lower than tropical macaques such as Macaca fascicu- markedly from October to January (Fig. 2), a high level laris: 66.7% (Yeager, 1996), M. nigra: 66% (O’Brien of young leaves was maintained in the diet of Assamese and Kinnaird, 1997), M. brunnescens: 90.4% (Andrews, macaques almost year-round. This can be mostly ac- 2003), and M. tonkeana: 76.7-84.4% (Riley, 2007), and counted for by the macaques feeding on young parts of more similar to temperate species such as Macaca fus- Indocalamus calcicolus (Rubiaceae) unexpanded leaves. cata yakui: 13% (Hanya, 2004) and M. mulatta: 9% This food item accounted for 77% of the Assamese ma- (Goldstein and Richard, 1989). The difference is, at caque young leaf diet, and formed the bulk of the diet in least partly, explained by the seasonal scarcity of fruit in most months. Probably, this plant species playes a cru- limestone habitats. Many studies have shown a strong cial role in the feeding ecology of Assamese macaques correlation between rainfall and fruit production in in limestone habitats. This bamboo is very abundant on limestone habitats, and that little fruit is available in the the cliffs and hilltops of limestone hills (Liang et al., dry season from October to March (Li and Roger, 2006; 1988), and unexpanded leaves eaten by macaques are Zhou et al., 2006). Thus, it seems that the lean period available almost year-round (personal observation). when fruit is uncommon is longer in this region than in Thus, they may provide a long-term stable food re- the tropics where fruit is more or less available year source for Assamese macaques in limestone habitats. round (Yeager, 1996; Riley, 2007). Furthermore, Assa- However, it is still unclear why the macaques show such mese macaques at Nonggang spent most maintenance a preference for the young parts of unexpanded leaves activities on the cliffs and hilltops of limestone hills from Indocalamus calcicolu. Obviously, more nutri- (unpublished data), which consist of bare rock, and are tional data are needed to compare these leaves with al- covered by small drought-enduring trees. Similarly, the ternatives. habitat of Assamese macaques in Nepal are character- Dietary flexibility may permit primates to live in a ized by steep slopes and rocky areas with patchy forest. variety of habitats. When high-quality food such as fruit They frequently forage in open bushy and shrubby lands is scarce, primates can use fiber-rich foods as fallback with low fruit availability (Chalise et al., 2003). This foods (Marshall and Wrangham, 2007). Accumulated further decreases fruit availability for Assamese ma- evidence shows the folivory of Macaca species (e.g. caques. Zhao, 1996; Hanya, 2004) is originally frugivorous. Within the genus Macaca, Assamese macaques at This dietary flexibility according to habitat may be one Nonggang rely on fiber-rich foods most heavily (77.4% of reasons why the genus Macaca is more widely dis- of the diet). This value is even higher than the average tributed than any other nonhuman primate genus. For of 24 species of colobines, which are forestomac- example, Japanese macaques can use a large amount of fermenting primates (52%, Kirkpatrick, 1999). Macaques mature leaves in response to long-term seasonal reduc- have an enlarged caecum and colon as the primary fer- tion in fruit in temperate regions (Hanya, 2004). Simi- mentation chamber, which enhances their digestive larly, there is a long lean period when fruit is uncom- abilities to digest large amounts of fiber-rich foods mon in limestone habitats. Monkeys may also need to (Lambert, 1998; Hayan, 2004). Our data and this develop the ability to cope with fiber-rich food so as to physiological fact suggest that Assamese macaques may survive in such environments. Although physiological have an ability to digest large amounts of fiber-rich food. investigation is needed, the fact that Assamese ma- Although Assamese macaques at Nonggang relied heav- caques rely heavily on leaves as fallback foods suggests ily on fibrous foods, they were mostly young leaves an adaptation that has allowed Assamese macaques to (95.7% of the total fibrous foods), and mature leaves survive in limestone habitats. accounted for only 4.3% of the total fibrous foods. This is similar to other folivorous primates (e.g Colobine: Acknowledgements This study was supported by the Na- young leaves account for 69% of the total fibrous foods, tional Nature Science Foundation of China (No 30860050), Kirkpatrick, 1999; Alouatta palliata: 87%, Estrada et al., Guangxi Science Foundation (0991095), Monitoring and 1999; Propithecus diadema: 65%-73%, Hemmingway, Conservation of Assamese macaques Project of National For- 1998). Compared with mature leaves, young leaves are estry Administration of China, Guangxi Beibu Gulf Serious preferred foods for primates because they have higher Specialization of Guangxi Natural Sciences Foundation ZHOU QH et al.: Diet of the Assamese macaque 25

(2010GXNSFE013004), and Project of Creative Team from Hemmingway CA, 1998. Selectivity and variability in the diet of Colleges and Universities in Guangxi. We thank the Guangxi Milne-Edwards’ sifakas Propithecus diadema edwardsi: Im- Forestry Bureau and Nonggang National Nature Reserve. We plications for folivory and seed-eating. International Journal also acknowledge the critical comments of two anonymous Primatology 19: 355–377. reviewers. Kirkpatrick RC, 1999. Colobine diet and social organization. In: Dolhinow P, Fuentes A ed. The Nonhuman Primates. Mountain References View, CA: Mayfield Publishing, 93–105. Lambert Je, 1998. Primate digestion: Interactions among anatomy, Ahsan MF, 1994. Feeding ecology of the primates of Bangladesh. physiology, and feeding ecology. Evolution Anthropology 7: In: Thierry B, Anderson RJ, Roeder JJ, Herrenschmidt N ed. 8–20. Current Primatology. Vol 1. Ecology and Evolution. Strasbourg: Li ZY, Rogers ME, 2006. Food items consumed by white-headed University of Louis Pasteur, 79–86. langurs in Fusui, China. International Journal of Primatology Altmann J, 1974. Observational study of behavior: Sampling 27: 1551–1567. methods. Behaviour 49: 227–262. Liang ZF, Liang JY, Liu LF, Mo XL, 1988. A report on vegetation Andrews K, 2003. Activity budgets and feeding behaviour of the in Nonggang Nature Reserve. Guangxi Botany (Supplement 1): buton macaque Macaca brunnecens. Master Thesis, Scotland: 83–184 (in Chinese). University of Aberdeen. Marshall AJ, Wrangham RW, 2007. Evolutionary consequences of Boonratana R, Chalise M, Das J, Htun S, Timmins RJ, 2008. fallback foods. International Journal of Primatology 28: Macaca assamensis. In: IUCN Red List Unit ed. IUCN 2010: 1219–1235. IUCN Red List of Threatened Species. Cambridge: IUCN Red O’Brien TG, Kinnaird MF, 1997. Behavior, diet and movements of List Unit, IUCN UK Office. the Sulawesi crested black macaque Macaca nigra. Interna- Caldecott JO, 1986. An ecological and behavioural study of the tional Journal of Primatology 18: 321–351. pig-tailed macaque. Contributions to Primatology 21: 1–286. Richard AF, 1985. Primates in Nature. New York: W. H. Freeman. Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder S, Riley EP, 2007. Flexibility in diet and activity patterns of Macaca 2007. Primates in Perspective. Oxford: Oxford University tonkeana in response to anthropogenic habitat alteration. Press. International Journal of Primatology 28: 107–133. Chalise MK, 2003. Assamese macaques Macaca assamensis in Shu ZM, Zhao TL, Huang QC, 1988. Vegetation survey in Nong- Nepal. Primate Conservation 19: 99–107. gang Nature Reserve. Guangxi Botany (supplement 1): Estrada A, Juan-solano S, Martinez TO, Coates-Estrada R, 1999. 185–214 (in Chinese) Feeding and general activity patterns of a howler monkey Yeager CP, 1996. Feeding ecology of the long-tailed macaque in Alouatta palliata troop living in a forest fragment at Los Ialimantan Tengah, Indonesia. International Journal of Prima- Tuxtlas, Mexico. American Journal of Primatology 48: tology 17: 51–62. 167–183. Yeager CP, Kool K, 2000. The behavioral ecology of Asian Colo- Goldstein SJ, Richard AF, 1989. Ecology of rhesus macaques bines. In: Whitehead PF, Jolly CJ ed. Colobine Monkeys: Their Macaca mulatta in northwest Pakistan. International Journal Ecology, Behaviour and Evolution. Cambridge, UK: Cam- Primatology 10: 531–567. bridge University Press, 251–284. Guangxi Forestry Department, 1993. Nature Reserves in Guangxi. Zhang YZ, Jin G, Quan GQ, Li Z, Ye F, et al., 1997. Distribution Beijing: China Forestry Publishing House (in Chinese). of Mammalian Species in China. Beijing: Chinese Forestry Hanya G, Noma N, Agetsuma N, 2003. Altitudinal and seasonal Publishing House. variations in the diet of Japanese macaques in Yakushima. Zhao QK, 1996. Etho-ecology of Tibetan macaques at Mount Primates 44: 51–59. Emei, China. In: Fa JE, Lindburg DG ed. Evolution and Ecol- Hanya G, 2004. Diet of a Japanese macaque troop in the conifer- ogy of Macaque Societies. Cambridge: Cambridge University ous forest of Yakushima. International Journal Primatology 25: Press, 263–289. 55–71. Zhou QH, Wei FW, Li M, Huang CM, Luo B, 2006. Diet and food Harris TR, Chapman CA, 2007. Variation in diet and ranging of choice of the François’ langur Trachypithecus francoisi in the black and white colobus monkeys in Kibale National Park, Nonggang Nature Reserve, China. International Journal of Uganda. Primates 48: 208–221. Primatology 27: 1441–1460.